Inference of relationships in the 'twilight zone' of homology using a combination of bioinformatics and site-directed mutagenesis: A case study of restriction endonucleases Bsp6I and PvuII

Nucleic Acids Research

Volumn 33, Issue 2, 2005, Pages 661-671

  Pawlak, Sebastian D ^b   Radlinska, Monika ^a   Chmiel, Agnieszka A ^b   Bujnicki, Janusz M ^b   Skowronek, Krzysztof J ^b  

^a UNIVERSITY OF WARSAW   (Poland)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

RESTRICTION ENDONUCLEASE; RESTRICTION ENDONUCLEASE BSP61; RESTRICTION ENDONUCLEASE PVUII; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; UNCLASSIFIED DRUG; AMINO ACID; DNA; ENDODEOXYRIBONUCLEASE FNU4HI; ENDODEOXYRIBONUCLEASE PVUII; MAGNESIUM;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; CATALYSIS; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; ENZYME ANALYSIS; ENZYME STRUCTURE; MOLECULAR RECOGNITION; PREDICTION; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FOLDING; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; STRUCTURAL GENOMICS; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; COMPARATIVE STUDY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; STRUCTURAL HOMOLOGY;

AMINO ACID SEQUENCE; AMINO ACIDS; CATALYSIS; CATALYTIC DOMAIN; CIRCULAR DICHROISM; COMPUTATIONAL BIOLOGY; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DIMERIZATION; DNA; MAGNESIUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY;

EID: 13844316471     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gki213     Document Type: Article

References (45)

1. Roberts,R.J., Belfort,M., Bestor,T., Bhagwat,A.S., Bickle,T.A., Bitinaite,J., Blumenthal,R.M., Degtyarev,S., Dryden,D.T., Dybvig,K. et al. (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res., 31, 1805-1812.
2. Wilson,G.G. and Murray,N.E. (1991) Restriction and modification systems. Annu. Rev. Genet., 25, 585-627.
3. Jeltsch,A., Kroger,M. and Pingoud,A. (1995) Evidence for an evolutionary relationship among type-II restriction endonucleases. Gene, 160, 7-16.
4. Bickle,T.A. and Kruger,D.H. (1993) Biology of DNA restriction. Microbiol. Rev., 57, 434-450.
5. Bujnicki,J.M. (2000) Phylogeny of the restriction endonuclease-like superfamily inferred from comparison of protein structures. J. Mol. Evol., 50, 39-44.
6. Bujnicki,J.M. (2001) Understanding the evolution of restriction-modification systems: clues from sequence and structure comparisons. Acta Biochim. Pol., 48, 935-967.
7. Pingoud,A. and Jeltsch,A. (2001) Structure and function of type II restriction endonucleases. Nucleic Acids Res., 29, 3705-3727.
8. Bujnicki,J.M. and Rychlewski,L. (2001) Grouping together highly diverged PD-(D/E)XK nucleases and identification of novel superfamily members using structure-guided alignment of sequence profiles. J. Mol. Microbiol. Biotechnol., 3, 69-72.
9. Pingoud,A. (2004) Restriction Endonucleases. Springer-Verlag, Berlin, Heidelberg,
10. Sapranauskas,R., Sasnauskas,G., Lagunavicius,A., Vilkaitis,G., Lubys,A. and Siksnys,V. (2000) Novel subtype of type IIs restriction enzymes. BfiI endonuclease exhibits similarities to the EDTA-resistant nuclease Nuc of Salmonella typhimurium. J. Biol. Chem. 275, 30878-30885.
11. Aravind,L., Makarova,K.S. and Koonin,E.V. (2000) SURVEY AND SUMMARY: holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res., 28, 3417-3432.
12. Bujnicki,J.M., Radlinska,M. and Rychlewski,L. (2001) Polyphyletic evolution of type II restriction enzymes revisited: two independent sources of second-hand folds revealed. Trends Biochem. Sci., 26, 9-11.
13. Saravanan,M., Bujnicki,J.M., Cymerman,I.A., Rao,D.N. and Nagaraja,V. (2004) Type II restriction endonuclease R.KpnI is a member of the HNH nuclease superfamily. Nucleic Acids Res., 32, 6129-6135.
14. Altschul,S.F., Madden,T.L., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
15. Kurowski,M.A. and Bujnicki,J.M. (2003) GeneSilico protein structure prediction meta-server. Nucleic Acids Res., 31, 3305-3307.
16. Kosinski,J., Cymerman,I.A., Feder,M., Kurowski,M.A., Sasin,J.M. and Bujnicki,J.M. (2003) A "FRankenstein's monster" approach to comparative modeling: merging the finest fragments ofFold-Recognition models and iterative model refinement aided by 3D structure evaluation. Proteins, 53 (Suppl. 6), 369-379.
17. Luthy,R., Bowie,J.U. and Eisenberg,D. (1992) Assessment of protein models with three-dimensional profiles. Nature, 356, 83-85.
18. Lubys,A. and Janulaitis,A. (1995) Cloning and analysis of the plasmid-borne genes encoding the Bsp6I restriction and modification enzymes. Gene, 157, 25-29.
19. Sambrook,J., Russell,D.W. and Sambrook,J. (2002) Molecular Cloning: A Laboratory Manual. 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Sreerama,N. and Woody,R.W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem., 287, 252-260.
21. Bujnicki,J.M. (2003) Crystallographic and bioinformatic studies on restriction endonucleases: inference of evolutionary relationships in the 'midnight zone' of homology. Curr. Protein Pept. Sci., 4, 327-337.
22. Kelley,L.A., MacCallum,R.M. and Stemberg,M.J. (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol., 299, 499-520.
23. Fischer,D. (2000) Hybrid fold recognition: combining sequence derived properties with evolutionary information. Pac. Symp. Biocomput 119-130.
24. Todone,F., Weinzierl,R.O., Brick,P. and Onesti,S. (2000) Crystal structure of RPB5, a universal eukaryotic RNA polymerase subunit and transcription factor interaction target. Proc. Natl Acad. Sci. USA 97, 6306-6310.
25. Lundstrom,J., Rychlewski,L., Bujnicki,J.M. and Elofsson,A. (2001) Pcons: a neural-network-based consensus predictor that improves fold recognition. Protein Sci., 10, 2354-2362.
26. Marti-Renom,M.A., Stuart,A.C., Fiser,A., Sanchez,R., Melo,F. and Sali,A. (2000) Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct., 29, 291-325.
27. Horton,J.R., Blumenthal,R.M. and Cheng,X. (2004) In Pingoud,A.M. (ed.), Restriction Endonucleases. Springer-Verlag, Berlin, Vol. 14, 361-392.
28. Cheng,X., Balendiran,K., Schildkraut,I. and Anderson,J.E. (1994) Structure of PvuII endonuclease with cognate DNA. EMBO J., 13, 3927-3935.
29. Nastri,H.G., Evans,P.D., Walker,I.H. and Riggs,P.D. (1997) Catalytic and DNA binding properties of PvuII restriction endonuclease mutants. J. Biol. Chem., 272, 25761-25767.
30. Horton,J.R. and Cheng,X. (2000) PvuII endonuclease contains two calcium ions in active sites. J. Mol. Biol., 300, 1049-1056.
31. Horton,J.R., Nastri,H.G., Riggs,P.D. and Cheng,X. (1998) Asp34 of PvuII endonuclease is directly involved in DNA minor groove recognition and indirectly involved in catalysis. J. Mol. Biol., 284, 1491-1504.
32. Eisenberg,D., Luthy,R. and Bowie,J.U. (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol., 277, 396-404.
33. Rice,M.R., Koons,M.D. and Blumenthal,R.M. (1999) Substrate recognition by the PvuII endonuclease: binding and cleavage of CAG5mCTG sites. Nucleic Acids Res., 27, 1032-1038.
34. Athanasiadis,A., Vlassi,M., Kotsifaki,D., Tucker,P.A., Wilson,K.S. and Kokkinidis,M. (1994) Crystal structure of PvuII endonuclease reveals extensive structural homologies to EcoRV. Nature Struct. Biol., 1, 469-475.
35. Selent,U., Ruter,T., Kohler,E., Liedtke,M., Thielking,V., Alves,J., Oelgeschlager,T., Wolfes,H., Peters,F. and Pingoud,A. (1992) A site-directed mutagenesis study to identify amino acid residues involved in the catalytic function of the restriction endonuclease EcoRV. Biochemistry, 31, 4808-4815.
36. Lagunavicius,A. and Siksnys,V. (1997) Site-directed mutagenesis of putative active site residues of MunI restriction endonuclease: replacement of catalytically essential carboxylate residues triggers DNA binding specificity. Biochemistry, 36, 11086-11092.
37. Pingoud,V., Sudina,A., Geyer,H., Bujnicki,J.M., Lurz,R., Luder,G., Morgan,R., Kubareva,E. and Pingoud,A. (2004) Specificity changes in the evolution of Type II restriction endonucleases: a biochemical and bioinformatic analysis of restriction enzymes that recognize unrelated sequences. J. Biol. Chem. First published on November 24, 2004, 10.1074/jbc.M409020200.
38. Venyaminov,S.Y. and Yang,J.T. (1996) In Fasman,G.D. (ed.), Circural Dichroism and the Conformational Analysis of Biomolecules, NY, pp. 69-106.
39. Huai,Q., Colandene,J.D., Chen,Y., Luo,F., Zhao,Y., Topal,M.D. and Ke,H. (2000) Crystal structure of NaeI - an evolutionary bridge between DNA endonuclease and topoisomerase. EMBO J., 19, 3110-3118.
40. Newman,M., Lunnen,K., Wilson,G., Greci,J., Schildkraut,I. and Phillips,S.E. (1998) Crystal structure of restriction endonuclease BglI bound to its interrupted DNA recognition sequence. EMBO J., 17 5466-5476.
41. Pingoud,V., Kubareva,E., Stengel,G., Friedhoff,P., Bujnicki,J.M., Urbanke,C., Sudina,A. and Pingoud,A. (2002) Evolutionary relationship between different subgroups of restriction endonucleases. J. Biol. Chem., 277, 14306-14314.
42. Bujnicki,J.M. (2001) A model of structure and action of Sau3AI restriction endonuclease that comprises two MufH-like endonuclease domains within a single polypeptide. Acta Microbiol. Pol., 50 219-231.
43. Bujnicki,J.M. and Rychlewski,L. (2001) Identification of a PD-(D/E)XK-like domain with a novel configuration of the endonuclease active site in the methyl-directed restriction enzyme Mrr and its homologs. Gene, 267, 183-191.
44. Pingoud,V., Conzelmann,C., Kinzebach,S., Sudina,A., Metelev,V., Kubareva,E., Bujnicki,J.M., Lurz,R., Luder,G., Xu,S.Y. et al. (2003) PspGI, a type II restriction endonuclease from the extreme thermophile Pyrococcus sp.: structural and functional studies to investigate an evolutionary relationship with several mesophilic restriction enzymes. J. Mol. Biol, 329, 913-929.
45. Rigden,D.J., Setlow,P., Setlow,B., Bagyan,I., Stein,R.A. and Jedrzejas,M.J. (2002) PrfA protein of Bacillus species: prediction and demonstration of endonuclease activity on DNA. Protein Sci., 11 2370-2381.